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Behavioural and electrophysiological responses of the female malaria mosquito Anopheles gambiae (Diptera: Culicidae) to Limburger cheese volatiles

Published online by Cambridge University Press:  10 July 2009

Bart G.J. Knols ,
Joop J.A. van Loon ,
Alan Cork ,
Rosemary D. Robinson ,
Wim Adam ,
Jocelijn Meijerink ,
Ruurd De Jong  and
Willem Takken
Bart G.J. Knols*
Affiliation:
Department of Entomology, Wageningen Agricultural University, The Netherlands:
Joop J.A. van Loon
Affiliation:
Department of Entomology, Wageningen Agricultural University, The Netherlands:
Alan Cork
Affiliation:
Natural Resources Institute, Chatham Maritime, Kent, ME4 4TB, UK
Rosemary D. Robinson
Affiliation:
Natural Resources Institute, Chatham Maritime, Kent, ME4 4TB, UK
Wim Adam
Affiliation:
Department of Entomology, Wageningen Agricultural University, The Netherlands:
Jocelijn Meijerink
Affiliation:
Department of Entomology, Wageningen Agricultural University, The Netherlands:
Ruurd De Jong
Affiliation:
Department of Entomology, Wageningen Agricultural University, The Netherlands:
Willem Takken
Affiliation:
Department of Entomology, Wageningen Agricultural University, The Netherlands:
*
*National Institute for Medical Research (Ifakara Centre), PO Box 53, Ifakara, Tanzania.
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Abstract

Limburger cheese, previously shown to attract female Anopheles gambiae Giles, was solvent extracted and chemically fractionated into acid and non-acid fractions. The extracts and aliquots of headspace odour of the cheese were analysed by gas chromatography and electron impact mass spectrometry. Nineteen saturated and unsaturated aliphatic fatty acids, ranging in carbon chain length from C2 to C18, were detected. The most abundant acids (>1 mg/g of cheese) identified in the acid extract were ethanoic, propanoic, butanoic, hexadecanoic and 9-octadecenoic acid. The same compounds were identified in analyses of headspace samples but only trace quantities of the less volatile acids (C10 to C16) were present, whilst C18 acids were absent. Behavioural responses of female A. gambiae towards a range of dilutions of the acid extract (in diethyl ether) were recorded in a windtunnel bioassay. The undiluted extract was found to be repellent, but became highly attractive (P «0.001) at lower doses, and was still significantly attractive (P<0.001) when diluted 106times. A synthetic mixture of 12 of the more abundant aliphatic acids identified in the acid extract was found to be significantly attractive (P<0.001) when diluted 108 times. Electroantennographic (EAG) studies showed significant and reproducible responses to (saturated) Limburger cheese headspace. At doses higher than 0.1%, the synthetic mixture of 12 acids elicited significantly higher EAG amplitudes than the solvent control (paraffin oil). EAG responses were recorded from mosquitoes stimulated with C5 to C8 acids, that were characterized by significant dose-dependencies. Weaker, though significant EAG responses were obtained with the less volatile acids (C9 to C14). Only hexadecanoic acid did not elicit a detectable response. The electrophysiological and behavioural responses obtained with fatty acids isolated from Limburger cheese suggests that together they could act as a kairomone for female A. gambiae. The implications of this are discussed together with the occurrence and bacterial production of these compounds on human skin.

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Type
Original Articles
Information
Bulletin of Entomological Research , Volume 87 , Issue 2 , April 1997 , pp. 151 - 159
Copyright
Copyright © Cambridge University Press 1997

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References

Acree, F., Turner, R.B., Gouck, H.K., Beroza, M. & Smith, N. (1968) L-lactic acid: a mosquito attractant isolated from humans. Science 161, 1346–1347.CrossRefGoogle ScholarPubMed
Anthony, R.M., Noble, W.C. & Pitcher, D.G. (1992) Characterization of aerobic non-lipophilic coryneforms from human feet. Clinical and Experimental Dermatology 17, 102–105.CrossRefGoogle ScholarPubMed
Bos, H.J. & Laarman, J.J. (1975) Guinea pig, lysine, cadaverine and estradiol as attractants for the malaria mosquito Anopheles Stephensi. Entomologia Experimentalis et Applicata 18, 161–172.CrossRefGoogle Scholar
Bursell, E., Gough, A.J.E., Beevor, S., Cork, A., Hall, D.R. & Vale, G.A. (1988) Identification of components of cattle urine attractive to tsetse flies, Glossina spp. (Diptera: Glossinidae). Bulletin of Entomological Research 78, 281–291.CrossRefGoogle Scholar
Carlson, D.A., Smith, N., Gouck, H.K. & Godwin, D.R. (1973) Yellow fever mosquitoes: Compounds related to lactic acid that attract females. Journal of Economic Entomology 66, 329–331.CrossRefGoogle Scholar
Cogan, T.M. & Daly, C. (1987) in Fox, P.F. (Ed.) Cheese: chemistry, physics and microbiology, Vol. 1. London, Elsevier Applied Science.Google Scholar
Coluzzi, M., Sabatini, A., Petrarca, V. & Di Deco, M.A. (1979) Chromosomal differentiation and adaptation to human environments in the Anopheles gambiae complex. Transactions of the Royal Society of Tropical Medicine and Hygiene 73, 483–497.CrossRefGoogle ScholarPubMed
Cork, A. (1994) Identification of electrophysiologically-active compounds for New World screwworm, Cochliotnyia hominivorax, in larval wound fluid. Medical and Veterinary Entomology 8, 151–159.CrossRefGoogle ScholarPubMed
Costantini, C., Gibson, G., Sagnon, N., Della Torre, A., Brady, J. & Coluzzi, M. (1996) Mosquito responses to carbon dioxide in a West African Sudan Savanna village. Medical and Veterinary Entomology. 10, 220–227.CrossRefGoogle Scholar
Davis, E.E. & Sokolove, P.G. (1976) Lactic acid sensitive receptors on the antennae of the mosquito Aedes aegypti. Journal of Comparative Physiology 105, 43–54.CrossRefGoogle Scholar
De Jong, C. & Badings, H.T. (1990) Determination of free fatty acids in milk and cheese. journal of High Resolution Chromatography 13, 94–98.CrossRefGoogle Scholar
De Jong, R. & Knols, B.G.J. (1995a) Selection of biting sites on man by two malaria mosquito species. Experientia 51, 80–84.CrossRefGoogle Scholar
De Jong, R. & Knols, B.G.J. (1995b) Olfactory responses of host-seeking Anopheles gambiae Giles (Diptera: Culicidae). Acta Tropica 59, 333–335.CrossRefGoogle ScholarPubMed
De Jong, R. & Knols, B.G.J. (1996) Selection of biting sites by mosquitoes. pp. 89–103in Cardew, G. (Ed.) Olfaction in mosquito-host interactions. Wiley, Chichester (Ciba foundation symposium 200).Google Scholar
Downing, D.Y., Strauss, J.S. & Pochi, P.E. (1969) Variability in the chemical composition of human skin surface lipids. Journal of Investigative Dermatology 53, 322–327.CrossRefGoogle ScholarPubMed
Fallis, A.M. & Smith, S.M. (1964) Ether extracts from birds and CO2 as attractants for some ornithophilic simuliids. Canadian Journal of Zoology 42, 723–730.CrossRefGoogle Scholar
Gillies, M.T. (1980) The role of carbon dioxide in host finding by mosquitoes (Diptera: Culicidae). Bulletin of Entomological Research 70, 525–532.CrossRefGoogle Scholar
Gillies, M.T. & Coetzee, M. (1987) A supplement to the Anophelinae of Africa South of the Sahara (Afrotropical region). 143 pp. Publications of the South African Institute for Medical Research, no. 55.Google Scholar
Gillies, M.T. & Wilkes, T.J. (1969) A comparison of the range of attraction of animal baits and of carbon dioxide for some West African mosquitoes. Bulletin of Entomological Research 59, 441–456.CrossRefGoogle ScholarPubMed
Gillies, M.T. & Wilkes, T.J. (1970) The range of attraction of single baits for some West African mosquitoes. Bulletin of Entomological Research 60, 225–235.CrossRefGoogle ScholarPubMed
Gillies, M.T. & Wilkes, T.J. (1974) The range of attraction of birds as baits for some West African mosquitoes (Diptera: Culicidae). Bulletin of Entomological Research 63, 573–581.CrossRefGoogle Scholar
Johns, D.L. (1958) Laboratory studies on olfaction in Glossina. Annual Report East African Trypanosomiasis Research Organisation 1958, 36–37.Google Scholar
Hall, D.R., Beevor, P.S., Cork, A., Nesbitt, B.F. & Vale, G.A. (1984) 1-Octen-3-ol: a potent olfactory stimulant and attractant for tsetse isolated from cattle odours. Insect Science and its Application 5, 335–339.Google Scholar
Hanspach, I. (1981) Untersuchungen über freie Fettsäuren als Aromasubstanzen verschiedener Käsesorten, PhD thesis, Justus-Liebig Universität, Giessen, pp. 124–127.Google Scholar
Hughes, J.C. (1957) Olfactory stimulation of tsetse flies and blowflies. Bulletin of Entomological Research 48, 561–579.CrossRefGoogle Scholar
Kanda, F., Yagi, E., Fukuda, M., Nakajima, K., Ohta, T. & Nakata, O. (1990) Elucidation of chemical compounds responsible for foot malodour. British Journal of Dermatology 122, 771–776.CrossRefGoogle ScholarPubMed
Knols, B.G.J. & De Jong, R. (1996) Limburger cheese as an attractant for the malaria mosquito Anopheles gambiae s.s. Parasitology Today 12, 159–161.CrossRefGoogle ScholarPubMed
Knols, B.G.J., De Jong, R. & Takken, W. (1994) Trapping system for testing olfactory responses of the malaria mosquito Anopheles gambiae in a windtunnel. Medical and Veterinary Entomology 8, 386–388.CrossRefGoogle Scholar
Knols, B.G.J., De Jong, R. & Takken, W. (1995) Differential attractiveness of isolated humans to mosquitoes in Tanzania. Transactions of the Royal Society of Tropical Medicine and Hygiene 89, 604–606.CrossRefGoogle ScholarPubMed
Krotozynski, B., Gabriel, G. & O'Neill, H. (1977) Characterization of human expired air: A promising investigative and diagnostic technique. Journal of Chromatographic Science 15, 239–244.CrossRefGoogle Scholar
Lacher, V. (1967) Elektrophysiologische untersuchungen an einzelnen Geruchsrezeptoren auf den Antennen weiblicher Moskitos (Aedes aegypti L.). Journal of Insect Physiology 13, 1461–1470.CrossRefGoogle Scholar
Larpent, J.P. (1989) Les fromages à pâte fraiche, molle, pressée ou persilée. pp. 206–231in Bourgeois, C.M. & Larpent, J.P. (Eds) Microbiologie alimentaire. Vol. 2., Les fermentations alimentaires. Technique et Documentation—Lavoisier.Google Scholar
Mackley, J.W. & Brown, H.E. (1984) Swormlure-4: A new formulation of the Swormlure-2 mixture as an attractant for adult screwworms, Cochliomyia hominivorax (Diptera: Calliphoridae). Journal of Economic Entomology 77, 1264–1268.CrossRefGoogle Scholar
Marshall, J., Holland, K.T. & Gribbon, E.M. (1988) A comparative study of the cutaneous microflora of normal feet with low and high levels of odour. Journal of Applied Bacteriology 65, 61–88.CrossRefGoogle ScholarPubMed
Mboera, L.E.G., Knols, B.G.J., Della Torre, A. & Takken, W. (1997) The response of Anopheles gambiae s.l. and A. funestus to tents baited with human odour or carbon dioxide in Tanzania. Bulletin of Entomological Research, 87, 173–178.CrossRefGoogle Scholar
Nicolaides, N. (1974) Skin lipids: Their biochemical uniqueness. Science 186, 19–26.CrossRefGoogle ScholarPubMed
Nicolaides, N., Fu, H.C. & Rice, G.R. (1968) The skin surface lipids of man compared with those of eighteen species of animals. Journal of Investigative Dermatology 51, 83–89.CrossRefGoogle ScholarPubMed
Pitcher, D.G. (1977) Rapid identification of cell wall components as a guide to the classification of aerobic coryneform bacteria from human skin. Journal of Medical Microbiology 10, 439–445.CrossRefGoogle Scholar
Pitcher, D.G. (1978) Aerobic cutaneous coryneforms: recent taxonomic findings. British Journal of Dermatology 98, 363–370.Google ScholarPubMed
Price, G.D., Smith, N. & Carlson, D.A. (1979) The attraction of female mosquitoes (Anopheles quadrimaculatus Say) to stored human emanations in conjunction with adjusted levels of relative humidity, temperature and carbon dioxide. Journal of Chemical Ecology 5, 383–395.CrossRefGoogle Scholar
Roessler, H.P. (1961) Versuche zur geruchlichen Anlockung weiblicher Stechmücken (Aedes aegypti L., Culicidae). Zeitschrift für vergleichende Physiologie 44, 184–231.CrossRefGoogle Scholar
Sastry, S.D., Buck, K.T., Janák, J., Dressler, M. & Preti, G. (1980) Volatiles emitted by humans. pp. 1086–1123in Waller, G.R. & Dermer, O.C. (Eds) Biochemical applications of mass spectrometry. New York, John Wiley & Sons Ltd.Google Scholar
Schreck, C.E., Smith, N., Carlson, D.A., Price, G.D., Haile, D. & Godwin, D.R. (1981) A material isolated from human hands that attracts female mosquitoes. Journal of Chemical Ecology 8, 429–438.CrossRefGoogle Scholar
Schreck, C.E., Kline, D.L. & Carlson, D.A. (1990) Mosquito attraction to substances from the skin of different humans. Journal of the American Mosquito Control Association 6, 406–410.Google ScholarPubMed
Sharpe, M.E., Law, B.A. & Phillips, B.A. (1977) Methanethiol production by coryneform bacteria: strains from dairy and human skin sources and Brevibacterium linens. Journal of General Microbiology 101, 345–349.CrossRefGoogle ScholarPubMed
Stoddart, D.M. (1990) The scented ape. Cambridge University Press.Google Scholar
Sutcliffe, J.F. (1987) Distance orientation of biting flies to their hosts. Insect Science and its Application 8, 611–616.Google Scholar
Takken, W. (1991) The role of olfaction in host-seeking of mosquitoes: a review. Insect Science and its Application 12, 287–295.Google Scholar
Takken, W. & Kline, D.L. (1989) Carbon dioxide and 1-octen-3-ol as mosquito attractants. Journal of the American Mosquito Control Association 5, 311–316.Google ScholarPubMed
Thomas, G., Schomaker, C.H., Been, T.H., Van den Berg, M.J. & Prijs, H.J. (1985) Host finding and feeding in Hydrotraea irritans (Diptera: Muscidae): the role of chemical senses. Veterinary Parasitology 18, 209–221.CrossRefGoogle ScholarPubMed
Thompson, B.H. (1976) Studies on the attraction of Simulium damnosum s.l. (Diptera: Simuliidae) to its hosts. Tropenmedizin und Parasitologie 27, 83–90.Google ScholarPubMed
Tonzetich, J. (1977) Production and origin of malodor: A review of mechanisms and methods of analysis. Journal of Periodontology 48, 13–20.CrossRefGoogle ScholarPubMed
Vale, G.A. (1980) Field studies on the responses of tsetse flies (Glossinidae) and other Diptera to carbon dioxide, acetone and other chemicals. Bulletin of Entomological Research 70, 563–570.CrossRefGoogle Scholar
Van Loon, J.J.A., Frentz, W.H. & Van Eeuwijk, F.A. (1992) Electroantennogram responses to plant volatiles in two species of Pieris butterflies. Entomologia Experimentalis et Applicata 62, 253–260.CrossRefGoogle Scholar
Wesley, E.K. & Musselwhite, M.S. (1975) Distribution and persistence of Staphylococcus and Micrococcus species and other bacteria on human skin. Applied Microbiology 30, 381–395.Google Scholar
White, G.B. (1974) Anopheles gambiae complex and disease transmission in Africa. Transactions of the Royal Society of Tropical Medicine and Hygiene 68, 278–299.CrossRefGoogle ScholarPubMed